Bottom Line:
Imidacloprid's systemic activity and mode of entry via roots or trunk injections reduce risk of environmental contamination and limit exposure of non-target organisms to pesticide residues.This is the first study to report the effects of pesticide applications on the arthropod communities in urban landscapes and demonstrate that imidacloprid increases spider mite fecundity through a plant-mediated mechanism.Widespread use of neonicotinoid insecticides, however, can disrupt ecosystems tipping the ecological balance in favor of herbivores and creating pest outbreaks.

Affiliation: Department of Entomology, University of Maryland, College Park, Maryland, United States of America. ada.s@tamu.edu

ABSTRACT

Background: Attempts to eradicate alien arthropods often require pesticide applications. An effort to remove an alien beetle from Central Park in New York City, USA, resulted in widespread treatments of trees with the neonicotinoid insecticide imidacloprid. Imidacloprid's systemic activity and mode of entry via roots or trunk injections reduce risk of environmental contamination and limit exposure of non-target organisms to pesticide residues. However, unexpected outbreaks of a formerly innocuous herbivore, Tetranychus schoenei (Acari: Tetranychidae), followed imidacloprid applications to elms in Central Park. This undesirable outcome necessitated an assessment of imidacloprid's impact on communities of arthropods, its effects on predators, and enhancement of the performance of T. schoenei.

Methodology/principal findings: By sampling arthropods in elm canopies over three years in two locations, we document changes in the structure of communities following applications of imidacloprid. Differences in community structure were mostly attributable to increases in the abundance of T. schoenei on elms treated with imidacloprid. In laboratory experiments, predators of T. schoenei were poisoned through ingestion of prey exposed to imidacloprid. Imidacloprid's proclivity to elevate fecundity of T. schoenei also contributed to their elevated densities on treated elms.

Conclusions/significance: This is the first study to report the effects of pesticide applications on the arthropod communities in urban landscapes and demonstrate that imidacloprid increases spider mite fecundity through a plant-mediated mechanism. Laboratory experiments provide evidence that imidacloprid debilitates insect predators of spider mites suggesting that relaxation of top-down regulation combined with enhanced reproduction promoted a non-target herbivore to pest status. With global commerce accelerating the incidence of arthropod invasions, prophylactic applications of pesticides play a major role in eradication attempts. Widespread use of neonicotinoid insecticides, however, can disrupt ecosystems tipping the ecological balance in favor of herbivores and creating pest outbreaks.

pone-0020018-g001: Effect of imidacloprid on arthropod communities and spider mite abundance in New York and Maryland.(A) Abundance of arthropods (per cm2 of leaf area) on imidacloprid-treated elms (N = 10) and on untreated trees (N = 10). Asterisks mark differences in overall abundance of arthropods that were significant within each year (P<0.05; Monte Carlo permutation test). At both locations, arthropod communities increased on elms that received imidacloprid. Abundance of spider mites, Tetranychidae, explained most of the variation due to imidacloprid treatments. Pie charts represent percent contribution of the most abundant taxa to the sampled arthropod community over three-year period at each location. (B) Abundance (√(number)/cm2) of the spider mite, T. schoenei, on elms treated with imidacloprid (N = 10) and on untreated trees (N = 10) in New York and Maryland. Asterisks mark means±s.e.m. that differed significantly (P<0.05). There was a significant interactive effect of treatment and time for both locations and in most years, and means were compared within each date (Table S1). Elevated densities of mites were found only on elms treated with imidacloprid. Rarely encountered taxa included arthropods in families Chrysopidae, Coccinellidae, Cecidomyiidae, Aphididae, Saproglyphidae and Thripidae. These arthropods were pooled and categorized as ‘Other’.

Mentions:
Owing to the fact that a federal agency mandated exactly which trees were treated with imidacloprid in Central Park, the random assignment of treatments was restricted. Therefore, inferences from preliminary surveys conducted in New York are interpreted conservatively and restricted only to trees in New York. Over the three years of this study, more than 254,990 arthropods were collected from the canopies of elms in New York and Maryland. Arachnids dominated communities of arboreal arthropods at both locations (Figure 1A). The less abundant taxa, grouped into ‘Other’ category, included Aphididae (aphids), Saproglyphidae (scavenger mites), Chrysopidae (green lacewings), Cecidomyiidae (predatory midges), Thripidae (thrips) and Coccinellidae (lady beetles in the genus Stethorus). Each taxon in this category was comprised of a small number of species, usually one or two, and did not differ significantly between trees treated with imidacloprid and untreated elms at either site. Eggs of Phytoseiidae and Chrysopidae were enumerated in addition to active stages of the predators, and eggs comprised 51% and 47% of all Phytoseiidae and Chrysopidae, respectively. We also captured other arthropods that did not account for more than 0.05% of all arthropods such as Anthocoridae, Araneae, Miridae, Reduvidae, and lepidopteran larvae among others.

pone-0020018-g001: Effect of imidacloprid on arthropod communities and spider mite abundance in New York and Maryland.(A) Abundance of arthropods (per cm2 of leaf area) on imidacloprid-treated elms (N = 10) and on untreated trees (N = 10). Asterisks mark differences in overall abundance of arthropods that were significant within each year (P<0.05; Monte Carlo permutation test). At both locations, arthropod communities increased on elms that received imidacloprid. Abundance of spider mites, Tetranychidae, explained most of the variation due to imidacloprid treatments. Pie charts represent percent contribution of the most abundant taxa to the sampled arthropod community over three-year period at each location. (B) Abundance (√(number)/cm2) of the spider mite, T. schoenei, on elms treated with imidacloprid (N = 10) and on untreated trees (N = 10) in New York and Maryland. Asterisks mark means±s.e.m. that differed significantly (P<0.05). There was a significant interactive effect of treatment and time for both locations and in most years, and means were compared within each date (Table S1). Elevated densities of mites were found only on elms treated with imidacloprid. Rarely encountered taxa included arthropods in families Chrysopidae, Coccinellidae, Cecidomyiidae, Aphididae, Saproglyphidae and Thripidae. These arthropods were pooled and categorized as ‘Other’.

Mentions:
Owing to the fact that a federal agency mandated exactly which trees were treated with imidacloprid in Central Park, the random assignment of treatments was restricted. Therefore, inferences from preliminary surveys conducted in New York are interpreted conservatively and restricted only to trees in New York. Over the three years of this study, more than 254,990 arthropods were collected from the canopies of elms in New York and Maryland. Arachnids dominated communities of arboreal arthropods at both locations (Figure 1A). The less abundant taxa, grouped into ‘Other’ category, included Aphididae (aphids), Saproglyphidae (scavenger mites), Chrysopidae (green lacewings), Cecidomyiidae (predatory midges), Thripidae (thrips) and Coccinellidae (lady beetles in the genus Stethorus). Each taxon in this category was comprised of a small number of species, usually one or two, and did not differ significantly between trees treated with imidacloprid and untreated elms at either site. Eggs of Phytoseiidae and Chrysopidae were enumerated in addition to active stages of the predators, and eggs comprised 51% and 47% of all Phytoseiidae and Chrysopidae, respectively. We also captured other arthropods that did not account for more than 0.05% of all arthropods such as Anthocoridae, Araneae, Miridae, Reduvidae, and lepidopteran larvae among others.

Bottom Line:
Imidacloprid's systemic activity and mode of entry via roots or trunk injections reduce risk of environmental contamination and limit exposure of non-target organisms to pesticide residues.This is the first study to report the effects of pesticide applications on the arthropod communities in urban landscapes and demonstrate that imidacloprid increases spider mite fecundity through a plant-mediated mechanism.Widespread use of neonicotinoid insecticides, however, can disrupt ecosystems tipping the ecological balance in favor of herbivores and creating pest outbreaks.

Affiliation:
Department of Entomology, University of Maryland, College Park, Maryland, United States of America. ada.s@tamu.edu

ABSTRACT

Background: Attempts to eradicate alien arthropods often require pesticide applications. An effort to remove an alien beetle from Central Park in New York City, USA, resulted in widespread treatments of trees with the neonicotinoid insecticide imidacloprid. Imidacloprid's systemic activity and mode of entry via roots or trunk injections reduce risk of environmental contamination and limit exposure of non-target organisms to pesticide residues. However, unexpected outbreaks of a formerly innocuous herbivore, Tetranychus schoenei (Acari: Tetranychidae), followed imidacloprid applications to elms in Central Park. This undesirable outcome necessitated an assessment of imidacloprid's impact on communities of arthropods, its effects on predators, and enhancement of the performance of T. schoenei.

Methodology/principal findings: By sampling arthropods in elm canopies over three years in two locations, we document changes in the structure of communities following applications of imidacloprid. Differences in community structure were mostly attributable to increases in the abundance of T. schoenei on elms treated with imidacloprid. In laboratory experiments, predators of T. schoenei were poisoned through ingestion of prey exposed to imidacloprid. Imidacloprid's proclivity to elevate fecundity of T. schoenei also contributed to their elevated densities on treated elms.

Conclusions/significance: This is the first study to report the effects of pesticide applications on the arthropod communities in urban landscapes and demonstrate that imidacloprid increases spider mite fecundity through a plant-mediated mechanism. Laboratory experiments provide evidence that imidacloprid debilitates insect predators of spider mites suggesting that relaxation of top-down regulation combined with enhanced reproduction promoted a non-target herbivore to pest status. With global commerce accelerating the incidence of arthropod invasions, prophylactic applications of pesticides play a major role in eradication attempts. Widespread use of neonicotinoid insecticides, however, can disrupt ecosystems tipping the ecological balance in favor of herbivores and creating pest outbreaks.